Nitric oxide and L-arginine metabolism in a devascularized porcine model of acute liver failure

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 303, Issue 3, 2012, Pages

  Sharma, Vikram ^a   ten Have, Gabriella A M ^b,c   Ytrebo, Lars ^e   Sen, Sambit ^a   Rose, Christopher F ^f   Neil Dalton, R ^d   Turner, Charles ^d   Revhaug, Arthur ^e   van Eijk, Hans M H ^c   Deutz, Nicolaas E P ^b,c   Jalan, Rajiv ^a   Mookerjee, Rajeshwar P ^a   Davies, Nathan A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d EVELINA LONDON CHILDREN S HOSPITAL   (United Kingdom)

^e UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^f UNIVERSITY OF MONTREAL   (Canada)

Author keywords

Arginase; Arginine; Asymmetric dimethylarginine

Indexed keywords

ARGINASE; ARGININE; CITRULLINE; GLUTAMINE; N(G),N(G) DIMETHYLARGININE; NITRIC OXIDE; ORNITHINE;

ACUTE LIVER FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD LEVEL; CONTROLLED STUDY; DEVASCULARIZATION; ENZYME ACTIVITY; FEMALE; INTESTINE; ISOTOPE LABELING; KIDNEY METABOLISM; MEASUREMENT; METABOLIC RATE; NONHUMAN; PRIORITY JOURNAL; SPLANCHNIC BLOOD FLOW; SWINE; SYNTHESIS;

ANIMALS; ARGINASE; ARGININE; CITRULLINE; DISEASE MODELS, ANIMAL; FEMALE; LIVER; LIVER FAILURE, ACUTE; NITRIC OXIDE; ORNITHINE; PORTACAVAL SHUNT, SURGICAL; SUS SCROFA;

EID: 84864759602     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00268.2011     Document Type: Article

References (52)

1. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J 357: 593-615, 2001.
2. Barbul A. Arginine and immune function. Nutrition 6: 53-58; discussion 59-62, 1990.
3. Barbul A, Lazarou SA, Efron DT, Wasserkrug HL, Efron G. Arginine enhances wound healing and lymphocyte immune responses in humans. Surgery 108: 331-336; discussion 336-337, 1990.
4. Bernal W, Auzinger G, Dhawan A, Wendon J. Acute liver failure. Lancet 376: 190-201, 2010.
5. Brusilow SW, Finkelstien J. Restoration of nitrogen homeostasis in a man with ornithine transcarbamylase deficiency. Metabolism 42: 1336-1339, 1993.
6. Cardounel AJ, Cui H, Samouilov A, Johnson W, Kearns P, Tsai AL, Berka V, Zweier JL. Evidence for the pathophysiological role of endogenous methylarginines in regulation of endothelial NO production and vascular function. J Biol Chem 282: 879-887, 2007.
7. Clemmesen JO, Kondrup J, Ott P. Splanchnic and leg exchange of amino acids and ammonia in acute liver failure. Gastroenterology 118: 1131-1139, 2000.
8. Das A, Hoare M, Davies N, Lopes AR, Dunn C, Kennedy PT, Alexander G, Finney H, Lawson A, Plunkett FJ, Bertoletti A, Akbar AN, Maini MK. Functional skewing of the global CD8 T cell population in chronic hepatitis B virus infection. J Exp Med 205: 2111-2124, 2008.
9. Davies NA, Hodges SJ, Pitsillides AA, Mookerjee RP, Jalan R, Mehdizadeh S. Hepatic guanylate cyclase activity is decreased in a model of cirrhosis: a quantitative cytochemistry study. FEBS Lett 580: 2123-2128, 2006.
10. Dejong CH, Kampman MT, Deutz NE, Soeters PB. Altered glutamine metabolism in rat portal drained viscera and hindquarter during hyperammonemia. Gastroenterology 102: 936-948, 1992.
11. Durante W, Johnson FK, Johnson RA. Arginase: a critical regulator of nitric oxide synthesis and vascular function. Clin Exp Pharmacol Physiol 34: 906-911, 2007.
12. Durante W, Liao L, Reyna SV, Peyton KJ, Schafer AI. Physiological cyclic stretch directs L-arginine transport and metabolism to collagen synthesis in vascular smooth muscle. FASEB J 14: 1775-1783, 2000.
13. Durante W, Liao L, Reyna SV, Peyton KJ, Schafer AI. Transforming growth factor-beta(1) stimulates L-arginine transport and metabolism in vascular smooth muscle cells: role in polyamine and collagen synthesis. Circulation 103: 1121-1127, 2001.
14. El-Gayar S, Thuring-Nahler H, Pfeilschifter J, Rollinghoff M, Bogdan C. Translational control of inducible nitric oxide synthase by IL-13 and arginine availability in inflammatory macrophages. J Immunol 171: 4561-4568, 2003.
15. Fliser D. Asymmetric dimethylarginine (ADMA): the silent transition from an 'uraemic toxin' to a global cardiovascular risk molecule. Eur J Clin Invest 35: 71-79, 2005.
16. Freund H, Atamian S, Holroyde J, Fischer JE. Plasma amino-acids as predictors of the severity and outcome of sepsis. Ann Surg 190: 571-576, 1979.
17. Hallemeesch MM, Ten Have GA, Deutz NE. Metabolic flux measurements across portal drained viscera, liver, kidney and hindquarter in mice. Lab Anim Care 35: 101-110, 2001.
18. Iber FL, Kerr DN, Dolle W, Sherlock S. Measurement of blood flow in the collateral vessels of the portal vein; preliminary results of a new method. J Clin Invest 39: 1201-1207, 1960.
19. Iyer RK, Yoo PK, Kern RM, Rozengurt N, Tsoa R, O'Brien WE, Yu H, Grody WW, Cederbaum SD. Mouse model for human arginase deficiency. Mol Cell Biol 22: 4491-4498, 2002.
20. Jalan R. Acute liver failure: current management and future prospects. J Hepatol 42 Suppl: S115-123, 2005.
21. Knorr A, Hirth-Dietrich C, Alonso-Alija C, Harter M, Hahn M, Keim Y, Wunder F, Stasch JP. Nitric oxide-independent activation of soluble guanylate cyclase by BAY 60-2770 in experimental liver fibrosis. Arzneim Forsch 58: 71-80, 2008.
22. Li H, Meininger CJ, Hawker JR, Haynes TE, Kepka-Lenhart D, Mistry SK, Morris SM, Wu GY. Regulatory role of arginase I and II in nitric oxide, polyamine, and proline syntheses in endothelial cells. Am J Physiol Endocrinol Metab 280: E75-E82, 2001.
23. Luiking YC, Hallemeesch MM, Vissers YLJ, Lamers WH, Deutz NEP. In vivo whole body and organ arginine metabolism during endotoxemia (sepsis) is dependent on mouse strain and gender. J Nutr 134: 2768s-2774s, 2004.
24. Mazziotti A, Bernardi M, Antonini L, Dioguardi FS, Bellusci R, Papa V, Tacconi C, Gasbarrini G, Cavallari A, Possati L. Plasma amino-acid patterns in experimental acute hepatic-failure-comparison between hepatectomy and liver devascularization in pigs. Surgery 90: 527-534, 1981.
25. Milewski PJ, Threlfall CJ, Heath DF, Holbrook IB, Wilford K, Irving MH. Intracellular free amino acids in undernourished patients with or without sepsis. Clin Sci (Lond) 62: 83-91, 1982.
26. Mookerjee RP, Dalton RN, Davies NA, Hodges SJ, Turner C, Williams R, Jalan R. Inflammation is an important determinant of levels of the endogenous nitric oxide synthase inhibitor asymmetric dimethylarginine (ADMA) in acute liver failure. Liver Transpl 13: 400-405, 2007.
27. Mookerjee RP, Malaki M, Davies NA, Hodges SJ, Dalton RN, Turner C, Sen S, Williams R, Leiper J, Vallance P, Jalan R. Increasing dimethylarginine levels are associated with adverse clinical outcome in severe alcoholic hepatitis. Hepatology 45: 62-71, 2007.
28. Morris SM Jr, Bhamidipati D, Kepka-Lenhart D. Human type II arginase: sequence analysis and tissue-specific expression. Gene 193: 157-161, 1997.
29. Nijveldt RJ, Teerlink T, Siroen MP, van Lambalgen AA, Rauwerda JA, van Leeuwen PA. The liver is an important organ in the metabolism of asymmetrical dimethylarginine (ADMA). Clin Nutr 22: 17-22, 2003.
30. Owen EE, Tyor MP, Flanagan JF, Berry JN. The kidney as a source of blood ammonia in patients with liver disease: the effect of acetazolamide. J Clin Invest 39: 288-294, 1960.
31. Palmer RM, Rees DD, Ashton DS, Moncada S. L-arginine is the physiological precursor for the formation of nitric oxide in endotheliumdependent relaxation. Biochem Biophys Res Commun 153: 1251-1256, 1988.
32. Poeze M, Bruins MJ, Kessels F, Luiking YC, Lamers WH, Deutz NE. Effects of L-arginine pretreatment on nitric oxide metabolism and hepatosplanchnic perfusion during porcine endotoxemia. Am J Clin Nutr 93: 1237-1247, 2011.
33. Russwurm M, Koesling D. NO activation of guanylyl cyclase. EMBO J 23: 4443-4450, 2004.
34. Schneider F, Lutun P, Boudjema K, Wolf P, Tempe JD. In vivo evidence of enhanced guanylyl cyclase activation during the hyperdynamic circulation of acute liver failure. Hepatology 19: 38-44, 1994.
35. Sen S, Rose CF, Ytrebo LM, Davies NA, Nedredal GI, Drevland SS, Kjonno M, Williams R, Butterworth RF, Revhaug A, Jalan R. Albumin dialysis reduces brain water and intracranial pressure in acute liver failure: a randomised controlled study in a pig model. Hepatology 38: 540A, 2003.
36. Shi O, Morris SM Jr, Zoghbi H, Porter CW, O'Brien WE. Generation of a mouse model for arginase II deficiency by targeted disruption of the arginase II gene. Mol Cell Biol 21: 811-813, 2001.
37. Ten Have GA, Bost MC, Suyk-Wierts JC, van den Bogaard AE, Deutz NE. Simultaneous measurement of metabolic flux in portally-drained viscera, liver, spleen, kidney and hindquarter in the conscious pig. Lab Anim Care 30: 347-358, 1996.
38. Tietge UJ, Bahr MJ, Manns MP, Boker KH. Plasma amino acids in cirrhosis and after liver transplantation: influence of liver function, hepatic hemodynamics and circulating hormones. Clin Transplant 16: 9-17, 2002.
39. Trewby PN, Williams R. Pathophysiology of hypotension in patients with fulminant hepatic failure. Gut 18: 1021-1026, 1977.
40. Ueda S, Yamagishi S, Okuda S. New pathways to renal damage: role of ADMA in retarding renal disease progression. J Nephrol 23: 377-386, 2010.
41. van Eijk HM, Luiking YC, Deutz NE. Methods using stable isotopes to measure nitric oxide (NO) synthesis in the L-arginine/NO pathway in health and disease. J Chromatogr B Analyt Technol Biomed Life Sci 851: 172-185, 2007.
42. van Eijk HM, Suylen DP, Dejong CH, Luiking YC, Deutz NE. Measurement of amino acid isotope enrichment by liquid chromatography mass spectroscopy after derivatization with 9-fluorenylmethylchloroformate. J Chromatogr B Analyt Technol Biomed Life Sci 856: 48-56, 2007.
43. Vockley JG, Jenkinson CP, Shukla H, Kern RM, Grody WW, Cederbaum SD. Cloning and characterization of the human type II arginase gene. Genomics 38: 118-123, 1996.
44. Wolfe R, Chinkes DL. Isotope Tracers in Metabolic Research: Principles and Practice of Kinetic Analysis. London, UK: Wiley, 2005.
45. Yagnik GP, Takahashi Y, Tsoulfas G, Reid K, Murase N, Geller DA. Blockade of the L-arginine/NO synthase pathway worsens hepatic apoptosis and liver transplant preservation injury. Hepatology 36: 573-581, 2002.
46. Yilmaz MI, Saglam M, Caglar K, Cakir E, Ozgurtas T, Sonmez A, Eyileten T, Yenicesu M, Acikel C, Oguz Y, Ozcan O, Bozlar U, Erbil K, Aslan I, Vural A. Endothelial functions improve with decrease in asymmetric dimethylarginine (ADMA) levels after renal transplantation. Transplantation 80: 1660-1666, 2005.
47. Ytrebo LM, Ingebrigtsen T, Nedredal GI, Elvenes OP, Korvald C, Romner B, Revhaug A. Protein S-100beta: a biochemical marker for increased intracranial pressure in pigs with acute hepatic failure. Scand J Gastroenterol 35: 546-551, 2000.
48. Ytrebo LM, Korvald C, Nedredal GI, Elvenes OP, Nielsen Grymyr OJ, Revhaug A. N-acetylcysteine increases cerebral perfusion pressure in pigs with fulminant hepatic failure. Crit Care Med 29: 1989-1995, 2001.
49. Ytrebo LM, Nedredal GI, Langbakk B, Revhaug A. An experimental large animal model for the assessment of bioartificial liver support systems in fulminant hepatic failure. Scand J Gastroenterol 37: 1077-1088, 2002.
50. Ytrebo LM, Sen S, Rose C, Davies NA, Nedredal GI, Fuskevaag OM, Ten Have GA, Prinzen FW, Williams R, Deutz NE, Jalan R, Revhaug A. Systemic and regional hemodynamics in pigs with acute liver failure and the effect of albumin dialysis. Scand J Gastroenterol 41: 1350-1360, 2006.
51. Ytrebo LM, Sen S, Rose C, Ten Have GA, Davies NA, Hodges S, Nedredal GI, Romero-Gomez M, Williams R, Revhaug A, Jalan R, Deutz NE. Interorgan ammonia, glutamate, and glutamine trafficking in pigs with acute liver failure. Am J Physiol Gastrointest Liver Physiol 291: G373-G381, 2006.
52. Zhang C, Hein TW, Wang W, Chang CI, Kuo L. Constitutive expression of arginase in microvascular endothelial cells counteracts nitric oxide-mediated vasodilatory function. FASEB J 15: 1264-1266, 2001.